Regulatory role of thiol isomerases in thrombus formation

References

• Ellgaard L, Ruddock LW. The human protein disulphide isomerase family: substrate interactions and functional properties. EMBO Rep. 2005;6:28–32.
   PubMed Web of Science ®Google Scholar
• Qin J, Clore GM, Gronenborn AM. The high-resolution three-dimensional solution structures of the oxidized and reduced states of human thioredoxin. Structure. 1994;2:503–522.
   PubMed Web of Science ®Google Scholar
• McArthur AG, Knodler LA, Silberman JD, et al. The evolutionary origins of eukaryotic protein disulfide isomerase domains: new evidence from the Amitochondriate protist Giardia lamblia. Mol Biol Evol. 2001;18:1455–1463.
   PubMed Web of Science ®Google Scholar
• Zhou J, Wu Y, Wang L, et al. The C-terminal CGHC motif of protein disulfide isomerase supports thrombosis. J Clin Invest. 2015;125:4391–4406.
   PubMed Web of Science ®Google Scholar
• Tian G, Xiang S, Noiva R, et al. The crystal structure of yeast protein disulfide isomerase suggests cooperativity between its active sites. Cell. 2006;124:61–73.
   PubMed Web of Science ®Google Scholar
• Weichsel A, Gasdaska JR, Powis G, et al. Crystal structures of reduced, oxidized, and mutated human thioredoxins: evidence for a regulatory homodimer. Structure. 1996;4:735–751.
   PubMed Web of Science ®Google Scholar
• Wang C, Li W, Ren J, et al. Structural insights into the redox-regulated dynamic conformations of human protein disulfide isomerase. Antioxid Redox Signal. 2013;19:36–45.
   PubMed Web of Science ®Google Scholar
• Song JL, Wang CC. Chaperone-like activity of protein disulfide-isomerase in the refolding of rhodanese. Eur J Biochem. 1995;231:312–316.
   PubMedGoogle Scholar
• Yao Y, Zhou Y, Wang C. Both the isomerase and chaperone activities of protein disulfide isomerase are required for the reactivation of reduced and denatured acidic phospholipase A2. Embo J. 1997;16:651–658.
   PubMed Web of Science ®Google Scholar
• Sliskovic I, Raturi A, Mutus B. Characterization of the S-denitrosation activity of protein disulfide isomerase. J Biol Chem. 2005;280:8733–8741.
   PubMed Web of Science ®Google Scholar
• Zai A, Rudd MA, Scribner AW, et al. Cell-surface protein disulfide isomerase catalyzes transnitrosation and regulates intracellular transfer of nitric oxide. J Clin Invest. 1999;103:393–399.
   PubMed Web of Science ®Google Scholar
• Cho J, Furie BC, Coughlin SR, et al. A critical role for extracellular protein disulfide isomerase during thrombus formation in mice. J Clin Invest. 2008;118:1123–1131.
   PubMed Web of Science ®Google Scholar
• Walczak CP, Tsai B. A PDI family network acts distinctly and coordinately with ERp29 to facilitate polyomavirus infection. J Virol. 2011;5:2386–2396.
   Google Scholar
• Wetterau JR, Combs KA, McLean LR, et al. Protein disulfide isomerase appears necessary to maintain the catalytically active structure of the microsomal triglyceride transfer protein. Biochemistry. 1991;30:9728–9735.
   PubMed Web of Science ®Google Scholar
• Jiang XM, Fitzgerald M, Grant CM, et al. Redox control of exofacial protein thiols/disulfides by protein disulfide isomerase. J Biol Chem. 1999;274:2416–2423.
   PubMed Web of Science ®Google Scholar
• Lindquist JA, Hammerling GJ, Trowsdale J. ER60/ERp57 forms disulfide-bonded intermediates with MHC class I heavy chain. Faseb J. 2001;15:1448–1450.
   PubMed Web of Science ®Google Scholar
• Kaiser BK, Yim D, Chow IT, et al. Disulphide-isomerase-enabled shedding of tumour-associated NKG2D ligands. Nature. 2007;447:482–486.
   PubMed Web of Science ®Google Scholar
• Sela M, White FH Jr., Anfinsen CB. Reductive cleavage of disulfide bridges in ribonuclease. Science. 1957;125:691–692.
   PubMed Web of Science ®Google Scholar
• Goldberger RF, Epstein CJ, Anfinsen CB. Acceleration of reactivation of reduced bovine pancreatic ribonuclease by a microsomal system from rat liver. J Biol Chem. 1963;238:628–635.
   PubMed Web of Science ®Google Scholar
• Laboissiere MC, Sturley SL, Raines RT. The essential function of protein-disulfide isomerase is to unscramble non-native disulfide bonds. J Biol Chem. 1995;270:28006–28009.
   PubMed Web of Science ®Google Scholar
• Appenzeller-Herzog C, Ellgaard L. The human PDI family: versatility packed into a single fold. Biochim Biophys Acta. 2008;1783:535–548.
   PubMed Web of Science ®Google Scholar
• Frand AR, Kaiser CA. Ero1p oxidizes protein disulfide isomerase in a pathway for disulfide bond formation in the endoplasmic reticulum. Mol Cell. 1999;4:469–477.
   PubMed Web of Science ®Google Scholar
• Lundstrom J, Holmgren A. Determination of the reduction-oxidation potential of the thioredoxin-like domains of protein disulfide-isomerase from the equilibrium with glutathione and thioredoxin. Biochemistry. 1993;32:6649–6655.
   PubMed Web of Science ®Google Scholar
• Alon A, Heckler EJ, Thorpe C, et al. QSOX contains a pseudo-dimer of functional and degenerate sulfhydryl oxidase domains. FEBS Lett. 2010;584:1521–1525.
   PubMed Web of Science ®Google Scholar
• Milev Y, Essex DW. Protein disulfide isomerase catalyzes the formation of disulfide-linked complexes of thrombospondin-1 with thrombin-antithrombin III. Arch Biochem Biophys. 1999;361:120–126.
   PubMed Web of Science ®Google Scholar
• Forster SJ, Freedman RB. Catalysis by protein disulphide-isomerase of the assembly of trimeric procollagen from procollagen polypeptide chains. Biosci Rep. 1984;4:223–229.
   PubMed Web of Science ®Google Scholar
• Di Jeso B, Park YN, Ulianich L, et al. Mixed-disulfide folding intermediates between thyroglobulin and endoplasmic reticulum resident oxidoreductases ERp57 and protein disulfide isomerase. Mol Cell Biol. 2005;25:9793–9805.
   PubMed Web of Science ®Google Scholar
• Bulleid NJ, Freedman RB. Defective co-translational formation of disulphide bonds in protein disulphide-isomerase-deficient microsomes. Nature. 1988;335:649–651.
   PubMed Web of Science ®Google Scholar
• LaMantia ML, Lennarz WJ. The essential function of yeast protein disulfide isomerase does not reside in its isomerase activity. Cell. 1993;74:899–908.
   PubMed Web of Science ®Google Scholar
• Hatahet F, Ruddock LW. Protein disulfide isomerase: a critical evaluation of its function in disulfide bond formation. Antioxid Redox Signal. 2009;11:2807–2850.
   PubMed Web of Science ®Google Scholar
• Dai Y, Wang C. A mutant truncated protein disulfide isomerase with no chaperone activity. J Biol Chem. 1997;272:27572–27576.
   PubMed Web of Science ®Google Scholar
• Uehara T, Nakamura T, Yao D, et al. S-nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration. Nature. 2006;441:513–517.
   PubMed Web of Science ®Google Scholar
• Shah CM, Bell SE, Locke IC, et al. Interactions between cell surface protein disulphide isomerase and S-nitrosoglutathione during nitric oxide delivery. Nitric Oxide. 2007;16:135–142.
   PubMed Web of Science ®Google Scholar
• Bell SE, Shah CM, Gordge MP. Protein disulfide-isomerase mediates delivery of nitric oxide redox derivatives into platelets. Biochem J. 2007;403:283–288.
   PubMed Web of Science ®Google Scholar
• Jasuja R, Furie B, Furie BC. Endothelium-derived but not platelet-derived protein disulfide isomerase is required for thrombus formation in vivo. Blood. 2010;116:4665–4674.
   PubMed Web of Science ®Google Scholar
• Thon JN, Peters CG, Machlus KR, et al. T granules in human platelets function in TLR9 organization and signaling. J Cell Biol. 2012;198:561–574.
   PubMed Web of Science ®Google Scholar
• Vaux D, Tooze J, Fuller S. Identification by anti-idiotype antibodies of an intracellular membrane protein that recognizes a mammalian endoplasmic reticulum retention signal. Nature. 1990;345:495–502.
   PubMed Web of Science ®Google Scholar
• Wan SW, Lin CF, Lu YT, et al. Endothelial cell surface expression of protein disulfide isomerase activates beta1 and beta3 integrins and facilitates dengue virus infection. J Cell Biochem. 2012;113:1681–1691.
   PubMed Web of Science ®Google Scholar
• Araujo TL, Zeidler JD, Oliveira PV, et al. Protein disulfide isomerase externalization in endothelial cells follows classical and unconventional routes. Free Radic Biol Med. 2017;103:199–208.
   PubMed Web of Science ®Google Scholar
• Marcus N, Shaffer D, Farrar P, et al. Tissue distribution of three members of the murine protein disulfide isomerase (PDI) family. Biochim Biophys Acta. 1996;1309:253–260.
   PubMedGoogle Scholar
• Gunther R, Srinivasan M, Haugejorden S, et al. Functional replacement of the Saccharomyces cerevisiae Trg1/Pdi1 protein by members of the mammalian protein disulfide isomerase family. J Biol Chem. 1993;268:7728–7732.
   PubMed Web of Science ®Google Scholar
• High S, Lecomte FJ, Russell SJ, et al. Glycoprotein folding in the endoplasmic reticulum: a tale of three chaperones? FEBS Lett. 2000;476:38–41.
   PubMed Web of Science ®Google Scholar
• Klappa P, Stromer T, Zimmermann R, et al. A pancreas-specific glycosylated protein disulphide-isomerase binds to misfolded proteins and peptides with an interaction inhibited by oestrogens. Eur J Biochem. 1998;254:63–69.
   PubMedGoogle Scholar
• Oliver JD, Van Der Wal FJ, Bulleid NJ, et al. Interaction of the thiol-dependent reductase ERp57 with nascent glycoproteins. Science. 1997;275:86–88.
   PubMed Web of Science ®Google Scholar
• Garbi N, Tanaka S, Momburg F, et al. Impaired assembly of the major histocompatibility complex class I peptide-loading complex in mice deficient in the oxidoreductase ERp57. Nat Immunol. 2006;7:93–102.
   PubMed Web of Science ®Google Scholar
• Holbrook LM, Watkins NA, Simmonds AD, et al. Platelets release novel thiol isomerase enzymes which are recruited to the cell surface following activation. Br J Haematol. 2010;148:627–637.
   PubMed Web of Science ®Google Scholar
• Holbrook LM, Sasikumar P, Stanley RG, et al. The platelet-surface thiol isomerase enzyme ERp57 modulates platelet function. J Thromb Haemost. 2012;10:278–288.
   PubMed Web of Science ®Google Scholar
• Wu Y, Ahmad SS, Zhou J, et al. The disulfide isomerase ERp57 mediates platelet aggregation, hemostasis, and thrombosis. Blood. 2012;119:1737–1746.
   PubMed Web of Science ®Google Scholar
• Kikuchi M, Doi E, Tsujimoto I, et al. Functional analysis of human P5, a protein disulfide isomerase homologue. J Biochem. 2002;132:451–455.
   PubMed Web of Science ®Google Scholar
• Passam FH, Lin L, Gopal S, et al. Both platelet- and endothelial cell-derived ERp5 support thrombus formation in a laser-induced mouse model of thrombosis. Blood. 2015;125:2276–2285.
   PubMed Web of Science ®Google Scholar
• Mazzarella RA, Srinivasan M, Haugejorden SM, et al. ERp72, an abundant luminal endoplasmic reticulum protein, contains three copies of the active site sequences of protein disulfide isomerase. J Biol Chem. 1990;265:1094–1101.
   PubMed Web of Science ®Google Scholar
• Kozlov G, Maattanen P, Schrag JD, et al. Structure of the noncatalytic domains and global fold of the protein disulfide isomerase ERp72. Structure. 2009;17:651–659.
   PubMed Web of Science ®Google Scholar
• Kramer B, Ferrari DM, Klappa P, et al. Functional roles and efficiencies of the thioredoxin boxes of calcium-binding proteins 1 and 2 in protein folding. Biochem J. 2001;357:83–95.
   PubMed Web of Science ®Google Scholar
• Chen K, Lin Y, Detwiler TC. Protein disulfide isomerase activity is released by activated platelets. Blood. 1992;79:2226–2228.
   PubMed Web of Science ®Google Scholar
• Essex DW, Chen K, Swiatkowska M. Localization of protein disulfide isomerase to the external surface of the platelet plasma membrane. Blood. 1995;86:2168–2173.
   PubMed Web of Science ®Google Scholar
• Chen K, Detwiler TC, Essex DW. Characterization of protein disulphide isomerase released from activated platelets. Br J Haematol. 1995;90:425–431.
   PubMed Web of Science ®Google Scholar
• Essex DW, Miller A, Swiatkowska M, et al. Protein disulfide isomerase catalyzes the formation of disulfide-linked complexes of vitronectin with thrombin-antithrombin. Biochemistry. 1999;38:10398–10405.
   PubMed Web of Science ®Google Scholar
• Falati S, Gross P, Merrill-Skoloff G, et al. Real-time in vivo imaging of platelets, tissue factor and fibrin during arterial thrombus formation in the mouse. Nat Med. 2002;8:1175–1181.
   PubMed Web of Science ®Google Scholar
• Chen VM, Ahamed J, Versteeg HH, et al. Evidence for activation of tissue factor by an allosteric disulfide bond. Biochemistry. 2006;45:12020–12028.
   PubMed Web of Science ®Google Scholar
• Ahamed J, Versteeg HH, Kerver M, et al. Disulfide isomerization switches tissue factor from coagulation to cell signaling. Proc Natl Acad Sci U S A. 2006;103:13932–13937.
   PubMed Web of Science ®Google Scholar
• Reinhardt C, Von Bruhl ML, Manukyan D, et al. Protein disulfide isomerase acts as an injury response signal that enhances fibrin generation via tissue factor activation. J Clin Invest. 2008;118:1110–1122.
   PubMed Web of Science ®Google Scholar
• Kim K, Hahm E, Li J, et al. Platelet protein disulfide isomerase is required for thrombus formation but not for hemostasis in mice. Blood. 2013;122:1052–1061.
   PubMed Web of Science ®Google Scholar
• Zhou J, May L, Liao P, et al. Inferior vena cava ligation rapidly induces tissue factor expression and venous thrombosis in rats. Arterioscler Thromb Vasc Biol. 2009;29:863–869.
   PubMed Web of Science ®Google Scholar
• Vandendries ER, Hamilton JR, Coughlin SR, et al. Par4 is required for platelet thrombus propagation but not fibrin generation in a mouse model of thrombosis. Proc Natl Acad Sci U S A. 2007;104:288–292.
   PubMed Web of Science ®Google Scholar
• Cho J, Kennedy DR, Lin L, et al. Protein disulfide isomerase capture during thrombus formation in vivo depends on the presence of beta3 integrins. Blood. 2012;120:647–655.
   PubMed Web of Science ®Google Scholar
• Lahav J, Jurk K, Hess O, et al. Sustained integrin ligation involves extracellular free sulfhydryls and enzymatically catalyzed disulfide exchange. Blood. 2002 Oct 1;100(7):2472–2478. PubMed PMID: 12239158. DOI:10.1182/blood-2001-12-0339
   PubMed Web of Science ®Google Scholar
• Lahav J, Wijnen EM, Hess O, et al. Enzymatically catalyzed disulfide exchange is required for platelet adhesion to collagen via integrin alpha2beta1. Blood. 2003;102:2085–2092.
   PubMed Web of Science ®Google Scholar
• Xiao T, Takagi J, Coller BS, et al. Structural basis for allostery in integrins and binding to fibrinogen-mimetic therapeutics. Nature. 2004;432:59–67.
   PubMed Web of Science ®Google Scholar
• Mor-Cohen R, Rosenberg N, Landau M, et al. Specific cysteines in beta3 are involved in disulfide bond exchange-dependent and -independent activation of alphaIIbbeta3. J Biol Chem. 2008;283:19235–19244.
   PubMed Web of Science ®Google Scholar
• Mor-Cohen R, Rosenberg N, Einav Y, et al. Unique disulfide bonds in epidermal growth factor (EGF) domains of beta3 affect structure and function of alphaIIbbeta3 and alphavbeta3 integrins in different manner. J Biol Chem. 2012;287:8879–8891.
   PubMed Web of Science ®Google Scholar
• O’Neill S, Robinson A, Deering A, et al. The platelet integrin alpha IIbbeta 3 has an endogenous thiol isomerase activity. J Biol Chem. 2000;275:36984–36990.
   PubMed Web of Science ®Google Scholar
• Ye F, Kim C, Ginsberg MH. Reconstruction of integrin activation. Blood. 2012;119:26–33.
   PubMed Web of Science ®Google Scholar
• Morrissey JH, Choi SH, Smith SA. Polyphosphate: an ancient molecule that links platelets, coagulation, and inflammation. Blood. 2012;119:5972–5979.
   PubMed Web of Science ®Google Scholar
• Sharda A, Kim SH, Jasuja R, et al. Defective PDI release from platelets and endothelial cells impairs thrombus formation in Hermansky-Pudlak syndrome. Blood. 2015;125:1633–1642.
   PubMed Web of Science ®Google Scholar
• Wynn R, Cocco MJ, Richards FM. Mixed disulfide intermediates during the reduction of disulfides by Escherichia coli thioredoxin. Biochemistry. 1995;34:11807–11813.
   PubMed Web of Science ®Google Scholar
• Qin J, Clore GM, Kennedy WM, et al. Solution structure of human thioredoxin in a mixed disulfide intermediate complex with its target peptide from the transcription factor NF kappa B. Structure. 1995;3:289–297.
   PubMed Web of Science ®Google Scholar
• Bowley SR, Fang C, Merrill-Skoloff G, et al. Protein disulfide isomerase secretion following vascular injury initiates a regulatory pathway for thrombus formation. Nat Commun. 2017;8:14151.
   PubMed Web of Science ®Google Scholar
• Barnes DW, Silnutzer J, See C, et al. Characterization of human serum spreading factor with monoclonal antibody. Proc Natl Acad Sci U S A. 1983;80:1362–1366.
   PubMed Web of Science ®Google Scholar
• Preissner KT, Reuning U. Vitronectin in vascular context: facets of a multitalented matricellular protein. Semin Thromb Hemost. 2011;37:408–424.
   PubMed Web of Science ®Google Scholar
• Seiffert D, Smith JW. The cell adhesion domain in plasma vitronectin is cryptic. J Biol Chem. 1997;272:13705–13710.
   PubMed Web of Science ®Google Scholar
• Reheman A, Gross P, Yang H, et al. Vitronectin stabilizes thrombi and vessel occlusion but plays a dual role in platelet aggregation. J Thromb Haemost. 2005;3:875–883.
   PubMed Web of Science ®Google Scholar
• Stopa JD, Baker KM, Grover SP, et al. Kinetic-based trapping by intervening sequence variants of the active sites of protein-disulfide isomerase identifies platelet protein substrates. J Biol Chem. 2017;292:9063–9074.
   PubMed Web of Science ®Google Scholar
• Sambrano GR, Huang W, Faruqi T, et al. Cathepsin G activates protease-activated receptor-4 in human platelets. J Biol Chem. 2000;275:6819–6823.
   PubMed Web of Science ®Google Scholar
• Korkmaz B, Moreau T, Gauthier F. Neutrophil elastase, proteinase 3 and cathepsin G: physicochemical properties, activity and physiopathological functions. Biochimie. 2008;90:227–242.
   PubMed Web of Science ®Google Scholar
• Stopa JD, Neuberg D, Puligandla M, et al. Protein disulfide isomerase inhibition blocks thrombin generation in humans by interfering with platelet factor V activation. JCI Insight. 2017;2:e89373.
   PubMed Web of Science ®Google Scholar
• Zucker M, Seligsohn U, Yeheskel A, et al. An allosteric disulfide bond is involved in enhanced activation of factor XI by protein disulfide isomerase. J Thromb Haemost. 2016;14:2202–2211.
   PubMed Web of Science ®Google Scholar
• Danishefsky KJ, Alexander RJ, Detwiler TC. Formation of a stable complex of thrombin and the secreted platelet protein glycoprotein G (thrombin-sensitive protein, thrombospondin) by thiol-disulfide exchange. Biochemistry. 1984;23:4984–4990.
   PubMed Web of Science ®Google Scholar
• Popescu NI, Lupu C, Lupu F. Extracellular protein disulfide isomerase regulates coagulation on endothelial cells through modulation of phosphatidylserine exposure. Blood. 2010;116:993–1001.
   PubMed Web of Science ®Google Scholar
• Furlan-Freguia C, Marchese P, Gruber A, et al. P2X7 receptor signaling contributes to tissue factor-dependent thrombosis in mice. J Clin Invest. 2011;121:2932–2944.
   PubMed Web of Science ®Google Scholar
• Schulman S, Bendapudi P, Sharda A, et al. Extracellular thiol isomerases and their role in thrombus formation. Antioxid Redox Signal. 2016;24:1–15.
   PubMed Web of Science ®Google Scholar
• Wang L, Wu Y, Zhou J, et al. Platelet-derived ERp57 mediates platelet incorporation into a growing thrombus by regulation of the alphaIIbbeta3 integrin. Blood. 2013;122:3642–3650.
   PubMed Web of Science ®Google Scholar
• Zhou J, Wu Y, Wang L, et al. The disulfide isomerase ERp57 is required for fibrin deposition in vivo. J Thromb Haemost. 2014;12:1890–1897.
   PubMed Web of Science ®Google Scholar
• Jordan PA, Stevens JM, Hubbard GP, et al. A role for the thiol isomerase protein ERP5 in platelet function. Blood. 2005;105:1500–1507.
   PubMed Web of Science ®Google Scholar
• Zhou J, Wu Y, Chen F, et al. The disulfide isomerase ERp72 supports arterial thrombosis in mice. Blood. 2017;130:817–828.
   PubMed Web of Science ®Google Scholar
• Holbrook L, Sandhar GK, Sasikumar P, et al. A humanized monoclonal antibody that inhibits platelet-surface ERp72 reveals a role for ERp72 in thrombosis. J Thromb Haemost. 2017;16:367–377.
   Web of Science ®Google Scholar
• Jasuja R, Passam FH, Kennedy DR, et al. Protein disulfide isomerase inhibitors constitute a new class of antithrombotic agents. J Clin Invest. 2012;122:2104–2113.
   PubMed Web of Science ®Google Scholar
• Geleijnse JM, Launer LJ, Van Der Kuip DA, et al. Inverse association of tea and flavonoid intakes with incident myocardial infarction: the Rotterdam Study. Am J Clin Nutr. 2002;75:880–886.
   PubMed Web of Science ®Google Scholar
• McCullough ML, Peterson JJ, Patel R, et al. Flavonoid intake and cardiovascular disease mortality in a prospective cohort of US adults. Am J Clin Nutr. 2012;95:454–464.
   PubMed Web of Science ®Google Scholar
• Flaumenhaft R, Furie B, Zwicker JI. Therapeutic implications of protein disulfide isomerase inhibition in thrombotic disease. Arterioscler Thromb Vasc Biol. 2015;35:16–23.
   PubMed Web of Science ®Google Scholar
• Lin L, Gopal S, Sharda A, et al. Quercetin-3-rutinoside Inhibits Protein Disulfide Isomerase by Binding to Its b’x Domain. J Biol Chem. 2015;290:23543–23552.
   PubMed Web of Science ®Google Scholar
• Bekendam RH, Bendapudi PK, Lin L, et al. A substrate-driven allosteric switch that enhances PDI catalytic activity. Nat Commun. 2016;7:12579.
   PubMed Web of Science ®Google Scholar
• Mandel R, Ryser HJ, Ghani F, et al. Inhibition of a reductive function of the plasma membrane by bacitracin and antibodies against protein disulfide-isomerase. Proc Natl Acad Sci U S A. 1993;90:4112–4116.
   PubMed Web of Science ®Google Scholar
• Khodier C, VerPlank L, Nag PP, et al. Identification of ML359 as a Small Molecule Inhibitor of Protein Disulfide Isomerase. Probe Reports from the NIH Molecular Libraries Program. Bethesda (MD)2010.
   Google Scholar
• Xu S, Sankar S, Neamati N. Protein disulfide isomerase: a promising target for cancer therapy. Drug Discov Today. 2014;19:222–240.
   PubMed Web of Science ®Google Scholar
• Voigtlaender M, Holstein K, Spath B, et al. Expression and release of platelet protein disulphide isomerase in patients with haemophilia A. Haemophilia. 2016;22:e537–e544.
   PubMed Web of Science ®Google Scholar
• Nagayama S, Yokoi T, Tanaka H, et al. Occurrence of autoantibody to protein disulfide isomerase in patients with hepatic disorder. J Toxicol Sci. 1994;19:163–169.
   PubMedGoogle Scholar
• Caorsi C, Niccolai E, Capello M, et al. Protein disulfide isomerase A3-specific Th1 effector cells infiltrate colon cancer tissue of patients with circulating anti-protein disulfide isomerase A3 autoantibodies. Transl Res. 2016;171(17–28):e1–2.
   PubMedGoogle Scholar